Coastal Coccolithophores (Guest Ed. R.W. Jordan)
J. Nannoplankton Res., Special Issue, 4, 2019, pp. 1–15 © 2019 International Nannoplankton Association
ISSN 1210-8049 Printed by The Sheridan Press, USA1

Seasonal succession of living coccolithophores in the
coastal waters of Tomari Port, Tottori, Japan
Kyoko Hagino-Tomioka*

Center for Advanced Marine Core Research, Kochi University, B200 Monobe, Nankoku, Kochi, 783-8502 Japan; *hagino@kochi-u.ac.jp

Natsuko Tomioka

Tosajuku Senior Highschool, Kita-nakayama 85, Kochi, 780-8026 Japan

Naotaka Tomioka

Kochi Institute for Core Sample Research, Japan Agency for Marine-Earth Science and Technology, 200 Monobe-otsu Nankoku, Kochi, 783-8502
Japan
Manuscript received 5th June, 2016; revised manuscript accepted 9th March, 2017

Abstract Seasonal changes in coccolithophore abundances and assemblage compositions were investigated in
the coastal waters of Tomari, Tottori, Japan from July 2007 to June 2014. The coccolithophores were less abundant in
winter, slightly increased in abundance in early to mid spring, and became rare/absent in late spring. They increased
again in early summer, but disappeared again from the studied area in mid to late summer, while sea-surface temperatures exceeded 28˚C. Coccolithophores flourished the most throughout autumn. This seasonal cycle in the abundanceof total coccolithophores was controlled by Emiliania huxleyi and Gephyrocapsa oceanica – the dominant species
in the nannofloras throughout the year. Braarudosphaera bigelowii and Tergestiella adriatica occurred in mid June,for only a short period (5–15 days), following the low abundance period in late spring. Species of Umbilicosphaeraand members of the Rhabdosphaeraceae appeared in early autumn. Middle to lower photic-zone dwellers, such as
Algirosphaera robusta, Oolithotus antillarum and Florisphaera profunda, appeared in the sea-surface samples of thestudied area only in mid to late autumn. Their occurrences indicate a weakening of water stratification in the studied
area during autumn.
Keywords Coastal coccolithophores, seasonality, Cretaceous/Palaeogene (K/Pg) boundary
1. Introduction
Coccolithophores are marine haptophytes that are characterised by calcareous scales called coccoliths. The Division Haptophyta that includes coccolithophores consistsof two classes – the Pavlovophyceae and Prymnesiophyceae – that are differentiated from each other based on
their cell, scale, flagella and haptonema morphologies(Green & Leadbeater, 1994). The Pavlovophyceae do nothave body scales, and are considered to be earlier-diverged
lineages of the haptophytes due to their relatively simple
morphologies and molecular phylogenetic positions (e.g.
de Vargas et al., 2007; Edvardsen et al., 2011). Membersof the Pavlovophyceae are distributed in both fresh andbrackish waters (Green, 1980). Most members of the
Prymnesiophyceae that produce organic body-scales havean affinity with coastal/neritic environments (e.g. de Vargas et al., 2007; Edvardsen et al., 2011). Other Prymnesiophyceae members that produce calcareous body-scales– the so-called coccolithophores – predominantly occur inoceanic environments (e.g. Young et al., 2003). These biogeographic, morphological and molecular phylogenetic
lines of evidence suggest that oceanic, calcifying cocco-

lithophores evolved from coastal non-calcifying Prymnesiophyceae (de Vargas et al., 2007).
Coccolithophores first appeared in the fossil recordin the Late Triassic, gradually diversifying through the
Mesozoic (Bown, 1987; Bown et al., 2004). At the Cretaceous/Paleogene (K/Pg) boundary mass extinction event,the oceanic Mesozoic species were eliminated, while thecoastal Mesozoic species survived selectively (Pospichal,
1996; Bown, 2005). The coastal survivors temporally
flourished in oceanic waters ‘immediately’ following theK/Pg boundary event; however, they once again became
constrained to coastal waters as newly-evolved Cenozoic
oceanic species appeared (Bown, 2005). The new Cenozoic taxa were predominantly oceanic, but some Cenozoic
species, such as placolith-bearing taxa, were distributed inboth coastal and pelagic waters (e.g. Young, 1994). Hence,
modern coastal coccolithophore assemblages are a mixture of species with Cenozoic and Mesozoic origins.
The floral compositions of pelagic coccolithophores
have been extensively studied in the Atlantic, northern
Indian and Central Pacific Oceans. They differ amongwater-masses (e.g. McIntyre & Bé, 1967; Okada & Hon-

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Hagino-Tomioka, Tomioka, Tomioka

jo, 1973; Kleijne, 1993), and(b)
(a)
100 moffshore change seasonally (e.g. Okada
samples& McIntyre, 1979; Reid, 1980;
Broerse, 2000; Cortés et al.,2001). Neritic coccolithophore
assemblages are relatively richin placolith-bearing species,st. 1
and usually poor in umbellist. 3
st. IshiwakiTomari Portform and floriform species (e.g.
st. 2
Japanst. B
st. A
Young, 1994). Quantitativest. Cfloristic studies on coastal cocTomari Portst. DTottori, Japanst. E
colithophores are scarce, andseasonal changes in coastal coc- Figure 1: (a) Location of Port Tomari, Tottori, Japan. (b) Sample localities along the coast and offshore
colithophores have only been of Port Tomari
reported from the Portuguese
and offshore of Tomari, from the fishing boat Ryoto-Maru,
Fig. 1 Hagino et al.
coast, facing the Atlantic Ocean(Silva et al., 2008), fromon 65 occasions, from July 2007 to July 2013 (see Hagino
Location of the Tomari port, Tottori, Japan (a) and locality of samples of coastal and offshore Tomari port (b).
the NW Mediterranean (e.g. Cros, 2002) and from certain
et al., 2015, app. 1). In order to confirm the seasonality
small bays of Andros Island, Aegean Sea, NE Mediterraof the coccolithophores recorded during the opportunisnean (Triantaphyllou et al., 2002; Dimiza et al., 2008).
tic sampling in 2007–2012, sampling was conducted
Successions of coccolithophores were recorded fromat Station 1 in Tomari Port at least once a month, fromthe coastal waters of Tomari, Tottori, Japan (Sea of Japan,
April 2012 to June 2014. Quantitative studies of the cocadjacent to the NW Pacific), over a six-year period, as part
colithophore assemblages were conducted by identifying
of a morphological and molecular phylogenetic study ofthe specimens preserved on filters under a cross-polarised
two coastal taxa with Mesozoic fossil records – Braarudolight microscope (LM). Selected filter samples were also
sphaera bigelowii and Tergestiella adriatica – (Hagino et
examined using a scanning electron microscope (SEM) inal., 2013, 2015, 2016). Occurrence data for all of the cocorder to evaluate the primary identifications made based
colithophore taxa in these samples were not discussed inon the optical microscopy (Plates 1–3). Preparation of thethese studies, however. Herein, we introduce the seasonalfilter samples for floristic and morphological studies, proity of the coccolithophores in the coastal waters of the Tocedures for the counting and identification of the coccomari area in order to better understand the characteristics
lithophores, and the method of calculation of cell densityof the coastal coccolithophore floras that have yielded B.
of the major coccolithophore taxa are fully described inbigelowii and T. adriatica. Differences in the occurrence
Hagino et al. (2015).
patterns among the typical Cenozoic and Mesozoic species of coccolithophores in the studied area are also dis2.2 Observation of living cells
cussed.
The 10-L seawater samples from the studied area wereprefiltered through a 50µm plankton net (Sefar Inc., DIN2. Materials and methods
110). The prefiltered samples were then concentrated us2.1 Floristic studies of coccolithophores
ing a piece of 1µm-mesh plankton net (Sefar Inc., NY1Surface seawater samples were originally collected for
HD). The motility of the major coccolithophore taxa inmorphological and molecular phylogenetic studies of B.
the concentrated seawater samples was examined under anbigelowii and T. adriatica in Tomari Port and offshore of
inverted LM, and then selected living cells were isolated
Tomari, Tottori Prefecture, Japan (Fig. 1; Hagino et al.,using a micropipette, placed on a 24-well culture plate
2013, 2015, 2016). Ten to 12L of seawater per sample
with MNK medium (Noël et al., 2004), and stored in awere collected, using a bucket, from the quay and break20˚C incubator under an 14:10 light:dark regime, in orderwaters of Tomari Port and from the Ishiwaki bathing
to grow them into clonal culture strains.
beach, on 167 occasions, from July 2007 to June 2014,

3

number of cells per litre

Seasonal succession of living coccolithophores

Figure 2: Seasonal changes in SSTs at (a) coastal and (b) offshore stations in the Tomari area, and seasonal changes in coccolithophore standing cropsin (c) coastal and (d) offshore samples from Tomari. Arrows with solid and open heads in (c) and (d) indicate declines in cell density in May andAugust, respectively

3. Sea-surface temperatures (SSTs) in
the Tomari area
The in situ SSTs of almost all of the coastal samples andsome of the offshore samples were measured using a bar
thermometer. The SSTs ranged from 27.0 to 30.5˚C insummer (mid July–September), and from 10 to 12˚C inwinter (January–February; Fig. 2a, b; Hagino et al., 2015,
app. 1).

4. Results
4.1 Total coccolithophore cell density
The coastal and offshore samples showed similar seasonal
successions of coccolithophore standing crops, although
the standing crops in the offshore samples were usuallyhigher than those in the coastal samples (Fig. 2c, d). The
standing crops at the coastal stations were usually <4000cells/L in winter (late December–February). Unfortu-

Hagino-Tomioka, Tomioka, Tomioka

number of cells per litre

4

Figure 3: Seasonal changes in abundance of major coccolithophore taxa at coastal and offshore stations, Tomari area. Arrows with solid and open
heads indicate a decline in cell density in May and August, respectively

Seasonal succession of living coccolithophores

nately, the coccolithophore abundances at the offshore
stations during this period are not available because sampling was difficult due to high waves caused by strong seasonal winds. The standing crop increased to 2000–20,000
cells/L at the coastal stations, and 20,000–80,000 cells/L at
the offshore stations, from March to early/mid May (Fig.
2c, d). The SSTs gradually increased from 13 to 16˚C overthis period (Fig. 2a, b).
The standing crop dropped to <2000 cells/L, or specimens were completely absent, at both coastal and offshore
stations from mid May through late May/early June (solid
arrows on Fig. 2c, d). In this period, the SSTs increased
from c.16 to 19˚C (Fig. 2a, b). The plankton net (50µm
mesh size) used for the prefiltration of the seawater samples always caught the bioluminescent dinoflagellate Noctiluca during this period. Also at this time, the seawater
was so transparent that the seafloor at Tomari Port was
clearly visible from the pier of the port. This suggests that
other phytoplankton (such as diatoms) were also rare.
Following the disappearance of Noctiluca, the coccolithophores recovered in abundance, occurring together
with abundant diatoms (e.g. Chaetoceros spp.), from mid
June to mid July. The plankton net used for seawater sample prefiltration was often clogged with Chaetoceros spp.,
and as a consequence of the relatively low water transparency, the seafloor in the port became invisible from thepier. During this period, the coccolithophore cell density
was usually >10,000 cells/L at the coastal stations and>20,000 cells/L at the offshore stations (Fig. 2c, d), andthe SSTs increased from 19 to 27˚C (Fig. 2a, b).
The cell density again dropped to <1000 cells/L at boththe coastal and offshore stations from mid July throughmid September, when the SST exceeded 28˚C (arrows with
open heads on Fig. 2c, d). The standing crops were highfrom late September through early December, typically
being >3000 cells/L at the coastal stations and >50,000
cells/L at the offshore stations (Fig. 2c, d), when the SSTs
gradually decreased from 26 to 13˚C (Fig. 2a, b).
4.2 Seasonal changes in major taxa at
TomariOf the 22 taxa identified under the LM (Hagino et al.,2015, app. 1), the following eight taxa exceeded 2000
cells/L at least once during the six-year study period:
Emiliania huxleyi, Gephyrocapsa oceanica, G. ericsonii,
B. bigelowii, T. adriatica, Syracosphaera spp., Algiros-

5

phaera robusta and Calciopappus rigidus.
Emiliania huxleyi and G. oceanica are the dominant
species in the studied area. Consequently, their seasonal
abundance changes almost equate to those of the total
coccolithophore assemblages. These species occurred atboth the coastal and offshore stations almost throughout
the year, but were rare (<2000 cells/L), or absent, during the period of Noctiluca occurrence (mid May to late
May/early June; solid arrows in Fig. 3a–d) and in mid tolate summer, when the SST exceeded 28˚C (mid July–mid
September; open arrows in Fig. 3a–d). The cell densityof these species was higher at the offshore stations thanat the coastal stations (Fig. 3a–d). Holococcolith-bearing
haploid cells of several coccolithophore taxa coexisted with E. huxleyi and G. oceanica at both the coastaland offshore stations, with very low abundances almost
throughout the year, except during the coccolithophorebarren period in late spring and mid to late summer (notillustrated).
The seasonal changes in the abundance of G. ericsonii resemble those of E. huxleyi and G. oceanica, being
abundant in occurrence in late June and in the autumn, butdiffer from those of E. huxleyi and G. oceanica in theirabsence/very low cell density in early spring (March toearly April; Fig. 3e, f). The cell density of G. ericsonii
was higher at the offshore stations than the coastal stations.
Braarudosphaera bigelowii and T. adriatica regularly
occurred, from mid June to early July, at both the coastaland offshore stations in 2008–2013 (Fig. 4a–d), following the coccolithophore-barren/low-density period frommid May through late May/early June (Fig. 2c, d). The
cell densities of these species were almost equivalent between the coastal and offshore locations, or were occasionally higher at the coastal sites than the offshore sites.
B. bigelowii and T. adriatica coexisted with E. huxleyi,
G. oceanica and G. ericsonii following the disappearanceof Noctiluca, but, unlike E. huxleyi, G. oceanica and G.
ericsonii, were absent from mid July through early Juneof the following year (Figs 3–4). The only exception was
one cell of B. bigelowii, found on 22 November, 2012 by
Hagino et al. (2013). In June 2014, multiple loose coccoliths of T. adriatica and loose pentaliths of B. bigelowii
were recorded from the coastal samples collected from
1–20 June and 15–18 June, respectively, but coccospheresof these taxa were not found in the final sample of this6

number of cells per litre

Hagino-Tomioka, Tomioka, Tomioka

Figure 4: Seasonal changes in abundance of major coccolithophore taxa in coastal and offshore stations, Tomari area. NB This figure is a duplicate
of Hagino et al. (2015, fig. 6)

study, collected on 25 June.
Syracosphaera spp. (mainly S. pulchra) occurredfrom late June or early July, and increased in abundance

mainly in early summer (mid June–early July) and in autumn (late September–November), but did not occur in
mid summer (mid July–mid September) or early springSeasonal succession of living coccolithophores(March–May; Fig. 5a, b; Hagino et al., 2015, app. 1). The
cell density of Syracosphaera spp. was usually higher atthe offshore stations than the coastal stations. The seasonal succession of Syracosphaera spp. resembles that ofG. ericsonii, but differs in the timing of its appearance inJune. G. ericsonii appeared in mid June, together with B.
bigelowii, T. adriatica, G. oceanica and E. huxleyi, while
Syracosphaera spp. usually occurred from late June, as
the numbers of B. bigelowii and T. adriatica declined(Hagino et al., 2015, app. 1).
Calciopappus rigidus occasionally occurred in theoffshore samples, typically in low abundances (<600cells/L) in autumn. It was usually absent from the coastal
sites, although it was exceptionally abundant in the port
on 30 June, 2011 (c. 48,000 cells/L; Fig. 5c, d; Hagino etal., 2015, app. 1).
Discosphaera tubifera, Rhabdosphaera stylifera, Umbilicosphaera foliosa and U. sibogae occurred as minor
species (<2000 cells/L) from late September to November (not illustrated; Hagino et al., 2015, app. 1). Following the occurrence of these taxa, A. robusta regularly occurred from October to the end of November, when the
SSTs decreased from 24 to 16˚C. The cell density of A.
robusta was higher in the offshore samples than the coastal samples (Figs 2a, b, 5e, f; Hagino et al., 2015, app. 1).
Florisphaera profunda, Helicosphaera walichii, Michaelsarsia sp., Oolithotus spp., Pontosphaera syracusana,
Scyphosphaera apsteinii, Reticulofenestra sessilis and/or
Ophiaster spp. often co-occurred with A. robusta in low
abundances (<2000 cells/L) in autumn (not illustrated;
Hagino et al., 2015, app. 1).
4.3 Observation of living cells
We checked the motility/non-motility of the cells of the
major coccolithophore taxa when isolating cells for theculture study, using an inverted LM. E. huxleyi, Calcidiscus leptoporus, C. quadriperforatus, G. ericsonii, G.
oceanica, R. sessilis, T. adriatica, U. foliosa and U. sibogae were non-motile, and did not possess flagellae or
haptonemas. B. bigelowii was non-motile, and did nothave a flagella, but did have a haptonema, which it uses
for adhesion to external substrates, as reported in Hagino
et al. (2016). The following nine taxa were motile, andeach had two flagellae and a haptonema: A. robusta, D.
tubifera, C. rigidus, H. wallichii, P. syracusana, S. apsteinii, R. stylifera, S. pulchra and unidentified holococco-

7lith-bearing taxa.
We established multiple clonal culture strains of E.
huxleyi, G. oceanica and S. pulchra from the coastal andoffshore waters of Tomari, but were not successful in culturing the other species.
4.4 SEM observation of selected species
We studied selected filters using an SEM in order to evaluate the identifications made in the LM, and to examine thedetailed morphologies of selected species. Plates 1 and 2
show the major taxa and selected minor species observedin this study, respectively. Plate 3 shows examples ofcomplete and collapsed specimens of F. profunda foundin this study. The calcareous scales (nannoliths) of F. profunda were very well preserved, and the protococcolithring-like basal structure that was discovered by Young etal. (2010) was observed in several nannoliths of a collapsed coccosphere (Pl. 3, fig. c).
5. Discussion
Coccolithophores occurred from mid June to early Julyand from late September through the following April, andexhibited seasonal abundance changes. They were veryrare or absent in mid to late summer (mid July throughmid September) and in late spring (mid May throughearly June; Fig. 2c, d). The scarce occurrence of coccolithophores in mid to late summer was probably due tohigh SSTs (>28˚C). This observation is consistent with theresults of Hagino et al. (2000) who reported that coccolithophores, especially E. huxleyi and G. oceanica, wererare in the surface-waters of the Western Pacific Warm
Pool, where SSTs exceeded 28˚C. On the other hand, thescarcity of coccolithophores from mid May to early June
was unexpected. The SSTs during this interval (16–19˚C)seem to be suitable for coccolithophore growth because
the temperatures are within the range where coccolithophores are common – before May (<16˚C) and after mid
June (>19˚C). Therefore, SST was not a major controlling
factor in the decrease in abundance of coccolithophores
during late spring.
The decrease in abundance of coccolithophores in latespring coincided with the appearance of Noctiluca spp.
This observation is consistent with those of previous studies that have shown a negative relationship in abundance
between Noctiluca scintillans and other phytoplankton.
The decrease in phytoplankton abundance during N. scin-

Hagino-Tomioka, Tomioka, Tomioka

number of cells per litre

8

Figure 5: Seasonal changes in abundance of major coccolithophore taxa in coastal and offshore stations, Tomari area

tillans bloom/abundant periods has been interpreted as being the result of high predation pressure by N. scintillans(e.g. Dharani et al., 2004; Mohamed & Mesaad, 2007).

These studies have also reported that blooms of N. scintillans resulted in a decrease in seawater pH due to the emission of CO2 by the respiration of N. scintillans. The sensi-

Seasonal succession of living coccolithophores

tivity of coccolithophores to the lowering of seawater pH
has been widely studied in the last decade, since the effects
of ongoing ocean acidification on marine calcifying organisms has been of great concern. Culture experiments haveshown that the calcification of coccoliths is affected byacidification, although the response varies among species,and even among strains in identical species (e.g. Langer etal., 2006, 2009; Iglesias-Rodríguez et al., 2008). Based on
the summation of previous experiments, Meyer & Riebesell (2015) concluded that acidification has a negative effect on the calcification and cellular particulate inorganic
to organic carbon ratios in E. huxleyi and G. oceanica. Because these two species are dominant in the studied area,
the change in pH, in tandem with the high occurrence ofNoctiluca, is possibly a controlling factor in the absence/scarcity of coccolithophores in late spring.
The compositions of the coccolithophore assemblages
changed seasonally (Fig. 6). A. robusta co-occurred withMichaelsarsia spp., Oolithotus antillarum, Ophiasterspp. and F. profunda from early October through December (Hagino et al., 2015, app. 1). All these species
are known to be middle to lower photic-zone dwellers
in stratified open-ocean locations (e.g. Okada & Honjo,
1973; Hagino et al., 2000; Cortés et al., 2001; Cros et al.,
2001; Dimiza et al., 2015), and so it was unexpected tofind these taxa regularly in the coastal surface-waters inthis study, since they were thought to be rare in the neritic
waters of the continental shelves (e.g. Young, 1994). In
this study, most specimens of A. robusta observed in theconcentrated seawater samples destined for the culture
study were motile (alive). We could not find any cells of
F. profunda in the concentrated seawater samples using
an inverted LM; therefore, it is unclear whether the F.
profunda cells observed in the filter samples with both across-polarised LM and SEM were actually alive in the
coastal surface waters. The presence of protococcolithring-like basal structures on the nannoliths of F. profunda(Pl. 3, fig. c), which are easily dissolved/lost during preservation (Young et al., 2010), however, suggests that theobserved specimens of F. profunda were likely living locally, and were not dead cells transported from a long
distance away.
The co-occurrence of these middle to lower photiczone dwellers in the surface-waters suggests that mixingof the water-column likely occurred in the studied area
in autumn. U. sibogae regularly appeared in low abun-

9

dances (<2000 cells/L) from late September, a few weeks
prior to the appearance of A. robusta (Hagino et al., 2015,
app. 1). U. sibogae is known to prefer moderately eutrophic conditions, between an upwelling centre and stratified oligotrophic waters (Hagino & Okada, 2004, 2006).

Therefore, the appearance of U. sibogae prior to the occurrence of middle to lower photic-zone taxa is likely
to indicate a weakening of stratification, starting in late
September.
Among the 22 taxa identified in the cross-polarised
LM, B. bigelowii and T. adriatica have Mesozoic fossil
records, whereas the remaining 20 taxa evolved in the
Cenozoic (Bown, 1987, 2005; Hagino et al., 2015). A
comparison of the cell densities of the major taxa among
the coastal and offshore stations showed that B. bigelowii
and T. adriatica were adapted to both coastal and neritic
waters, while the other 20 taxa preferred offshore waters
to coastal ones, although they do live in coastal waters,
but in significantly lower abundances.
These results confirm the findings of previous studies– that K/Pg survivors had an affinity for coastal environments, while typical Cenozoic coccolithophores preferredoceanic waters (e.g. Young et al., 2003; Bown, 2005).
Here, B. bigelowii and T. adriatica occurred regularly in
mid June to late June/early July during the SST increase
from 19 to 26˚C, but they did not occur in autumn, when
the SSTs decreased from 26 to 19˚C. The factors inducing
their co-occurrence in early summer are still uncertain, as
discussed in Hagino et al. (2015); however, their specificoccurrence patterns, their short-lived flourishes after theintervals of absent/rare oceanic taxa, are reminiscent of
the episodic high abundances of coastal K/Pg survivors,
including B. bigelowii and the ancestor of T. adriatica,
after the extinction of the majority of Mesozoic oceanic
taxa following the K/Pg event.
One of the possible mechanisms that could havecaused the selective extinction of oceanic calcareous nannoplankton is a short-lived ocean acidification interval
after the K/Pg event (e.g. D’Hondt et al., 1994; Alegret
et al., 2012; Ohno et al., 2014). Blooms of Noctiluca cancause episodic decreases in the pH of surface seawater(Dharani et al., 2004; Mohamed & Mesaad, 2007). This
could explain the lowered abundances of E. huxleyi andG. oceanica, which are sensitive to water acidification(e.g. Meyer & Riebesell, 2015), in the Tomari area duringlate spring. Here, we propose a working hypothesis for10

Hagino-Tomioka, Tomioka, Tomioka

neritic–oceanic taxa with Cenozoic origins
neritic-oceanic taxa with Cenozoic origin

SST >28˚C

middle–lower
photic-zone dwellers

Tergestiella adriatica

coastal specialists with Mesozoic origins

Figure 6: Schematic diagram showing the seasonal succession of coccolithophores in the Tomari area

the occurrence of the Mesozoic coastal taxa B. bigelowii
and T. adriatica in mid June that involves them being
triggered by a decrease in their competitors (E. huxleyi
and G. oceanica), likely related to the abundance of Noctiluca spp. In order to confirm this hypothesis, further
studies on seasonal changes in hydrographic conditions,as well as in the total plankton community, in the Tomari
area will be necessary.
Acknowledgements
We thank Takayuki Tanaka and Kayo Tanaka for help with theReferences
Alegret, L., Thomas, E. & Lohmann, K.C. 2012. End-Cretaceous
marine mass extinction not caused by productivity collapse.

Proceedings of the National Academy of Sciences, 109(3):728–732.

Bown, P.R. 1987. Taxonomy, evolution, and biostratigraphy of

Late Triassic-Early Jurassic calcareous nannofossils. Special
Papers in Palaeontology, 38: 118 pp.

Bown, P.R. 2005. Selective calcareous nannoplankton survivor-

ship at the Cretaceous–Tertiary boundary. Geology, 33(8):653–656.

sampling at Tomari, Tottori, Japan. We also thank Hisatake

Bown, P.R., Lees, J.A. & Young, J.R. 2004. Calcareous nan-

Prof Maria Triantaphyllou (University of Athens), an anony-Thierstein & J.R. Young (Eds). Coccolithophores - From mo-

Okada for his suggestions on this manuscript. We acknowledge
mous reviewer, Prof Ric Jordan (Yamagata University) and Dr

Jamie Shamrock for their critical reviews and suggestions. This

research was supported by a grant-in-aid for the environmental
study of art and sciences from the Tottori Prefecture, Japan, andanother for scientific research from the Japan Society for the Promotion of Sciences (Nos 26400505 and 90374206).

noplankton evolution and diversity through time. In: H.R.
lecular processes to global impact. Springer-Verlag, Berlin/
Heidelberg: 481–508.

Broerse, A.T.C. 2000. Coccolithophore export production in se-lected ocean environments. PhD thesis, Free University Amsterdam, Amsterdam: 185 pp.

Cortés, M.Y., Bollmann, J. & Thierstein, H.R. 2001. Coccolithophore ecology at the HOT station ALOHA Hawaii. DeepSea Research. Part 2, Topical Studies in Oceanography, 48:

Seasonal succession of living coccolithophores

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Plate 1
SEM images of major coccolithophore species observed in this study
a. Emiliania huxleyi
st. 3, 27 June, 2009

d. Braarudosphaera bigelowii
st. D
15 June, 2012b. Gephyrocapsa oceanica
st. 1, 27 May, 2012

c. Gephyrocapsa ericsonii, st. 3, 27 June, 2009e. Tergestiella adriatica
offshore of Tomari
17 June, 2012

f. Calciopappus rigidus
offshore of Tomari
25 November, 2012

g. Syracosphaera pulchra
culture strain TMR-18
isolated from seawater
8 August, 2011h. Algirosphaera robusta
offshore of Tomari
12 October, 2012

12

Hagino-Tomioka, Tomioka, Tomioka

Plate 2
SEM images of selected minor coccolithophore species observed in this study
b. Syracosphaera tumularis, offshore of Tomari, 25 November, 2012

a. Calciosolenia murrayi
offshore of Tomari
25 November, 2012

c. Syracosphaera bannockii
offshore of Tomari
17 June, 2012

d. Syracosphaera molischii
offshore of Tomari, 23 June, 2012

g. Syracosphaera rotula
offshore of Tomari
4 October, 2012

f. Syracosphaera anthos
offshore of Tomari
25 November, 2012
e. Syracosphaera ossa
offshore of Tomari
12 October, 2012h. Syracosphaera corolla
offshore of Tomari, 12 October, 2012

i. Cyrtosphaera aculeata
offshore of Tomari
23 June, 2012

j. Acanthoica quattrospina
st. D in Tomari Port
26 June, 2012

Seasonal succession of living coccolithophores

13

Plate 3
SEM images of Florisphaera profunda, offshore of Tomari, 10 October, 2012

collapsed specimen

intact coccosphereclose-up of ﬁg. b

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